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Involvement of membrane degradation in response to oleocellosis induced by exogenous orange oil in citrus fruit

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Abstract

Navel oranges (Citrus sinensis L. Osbeck) were treated with pure orange oil to simulate the natural cause of oleocellosis and to elucidate the mechanism involving in fruit injury caused by orange oil. Results showed that no injury was found on the rind surface of control fruits during storage. By contrast, application of exogenous orange oil onto the surface of fruits could rapidly induce peel injury. Moreover, the severity of injury increased during storage. At the end of the storage time, the collapse and discolouration scores were 17.3 and 16.7 times higher than those at 4 h after treatment. Oil treatment caused fruit membrane degradation by increasing the activities of phospholipase D and lipoxygenase, reducing the ratio of unsaturated/saturated fatty acids and enhancing the levels of hydrogen peroxide, superoxide anion, malonaldehyde, and electrolyte leakage. In addition, the treatment reduced the activities of superoxide dismutase and catalase, as well as suppressed the ascorbate acid–glutathione cycle, which led to the efficiency loss of the reactive oxygen species scavenging system.

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Abbreviations

PLD:

Phospholipase D

PC:

Phosphatidylcholine

PI:

Phosphatidylinositol

PA:

Phosphatidic acid

ROS:

Reactive oxygen species

H2O2 :

Hydrogen peroxide

O2· :

Superoxide anion

LOX:

Lipoxygenase

MDA:

Malonaldehyde

CAT:

Catalase

SOD:

Superoxide dismutase

POD:

Peroxidase

APX:

Ascorbate peroxidase

GR:

Glutathione reductase

AsA:

Ascorbate acid

GSH:

Glutathione

References

  • Aghdam MS, Mohammadkhani N (2014) Enhancement of chilling stress tolerance of tomato fruit by postharvest brassinolide treatment. Food Bioprocess Technol 7:909–914

    Article  CAS  Google Scholar 

  • Agustí M, Almela V, Juan M, Alferez F, Tadeo FR, Zacarías L (2001) Histological and physiological characterization of rind breakdown of ‘Navelate’ sweet orange. Ann Bot-London 88:415–422

    Article  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bang DY, Byeon SK, Moon MH (2014) Rapid and simple extraction of lipids from blood plasma and urine for liquid chromatography-tandem mass spectrometry. J Chromatogr A 1331:19–26

    Article  CAS  PubMed  Google Scholar 

  • Brehe JE, Burch HB (1976) Enzymatic assay for glutathione. Anal Biochem 74:189–197

    Article  CAS  PubMed  Google Scholar 

  • Cao S, Yang Z, Cai Y, Zheng Y (2011) Fatty acid composition and antioxidant system in relation to susceptibility of loquat fruit to chilling injury. Food Chem 127:1777–1783

    Article  CAS  Google Scholar 

  • Cronjé PJR, Barry GH, Huysamer M (2011) Postharvest rind breakdown of ‘Nules Clementine’ mandarin is influenced by ethylene application, storage temperature and storage duration. Postharvest Biol Technol 60:192–201

    Article  Google Scholar 

  • Cronjé PJR, Zacarías L, Alférez F (2017) Susceptibility to postharvest peel pitting in Citrus fruits as related to albedo thickness, water loss and phospholipase activity. Postharvest Biol Technol 123:77–82

    Article  Google Scholar 

  • de Barros ÉA, Broetto F, Bressan DF, Sartori MM, Costa VE (2014) Chemical composition and lipoxygenase activity in soybeans (Glycine max L. Merr.) submitted to gamma irradiation. Radiat Phys Chem 98:29–32

  • Dhindsa RS, Plumb-Dhindsa P, Thorpe TA (1981) Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J Exp Bot 32:93–101

    Article  CAS  Google Scholar 

  • Fischer IH, Toffano L, Lourenço S, Amorim L (2007) Caracterização dos danos pós-colheita em citros procedentes de “packinghouse”. Fitopatol Bras 32:304–310

    Article  Google Scholar 

  • Jones E, Hughes RE (1983) Foliar ascorbic acid in some angiosperms. Phytochemistry 22:2493–2499

    Article  CAS  Google Scholar 

  • Knight TG, Klieber A, Sedgley M (2001) The relationship between oil gland and fruit development in Washington Navel orange (Citrus sinensis L. Osbeck). Ann Bot 88:1039–1047

    Article  Google Scholar 

  • Knight TG, Klieber A, Sedgley M (2002) Structural basis of the rind disorder oleocellosis in Washington navel orange (Citrus sinensis L. Osbeck). Ann Bot 90:765–773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’orange ovular callus lines. Plant Cell Physiol 18:463–467

    Article  CAS  Google Scholar 

  • Li M, Hong Y, Wang X (2009) Phospholipase D- and phosphatidic acid-mediated signaling in plants. Biochem Biophys Acta 1791:927–935

    CAS  PubMed  Google Scholar 

  • Liu H, Song L, You Y, Li Y, Duan X, Jiang Y, Ashrafd M, Lu W (2011) Cold storage duration affects litchi fruit quality, membrane permeability, enzyme activities and energy charge during shelf time at ambient temperature. Postharvest Biol Technol 60:24–30

    Article  CAS  Google Scholar 

  • Liu LD, Ming J, Zeng KF, Liao C (2012) Effect of postharvest polyamines treatment on oleocellosis of valencia oranges. AMM 140:324–328

    Article  CAS  Google Scholar 

  • Magwaza LS, Opara UL, Terry LA, Landahl S, Cronje PJ, Nieuwoudt H, Mouazen AM, Saeys W, Nicolaï BM (2012) Prediction of ‘Nules Clementine’ mandarin susceptibility to rind breakdown disorder using Vis/NIR spectroscopy. Postharvest Biol Technol 74:1–10

    Article  CAS  Google Scholar 

  • Mao LC, Wang GZ, Zhu CG, Pang HQ (2007) Involvement of phospholipase D and lipoxygenase in response to chilling stress in postharvest cucumber fruits. Plant Sci 172:400–405

    Article  CAS  Google Scholar 

  • Mirdehghan SH, Rahemi M, Martínez-Romero D, Guillén F, Valverde JM, Zapata PJ, Serrano M, Valero D (2007) Reduction of pomegranate chilling injury during storage after heat treatment: role of polyamines. Postharvest Biol Technol 44:19–25

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Montero CRS, Schwarz LL, dos Santos LC, dos Santos RP, Bender RJ (2012) Oleocellosis incidence in citrus fruit in response to mechanical injuries. Sci Hortic-Amsterdam 134:227–231

    Article  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Paliyath G, Droillard MJ (1992) The mechanisms of membrane deterioration and disassembly during senescence. Plant Physiol Biochem 30:789–812

    CAS  Google Scholar 

  • Patterson BD, MacRae EA, Ferguson IB (1984) Estimation of hydrogen peroxide in plant extracts using titanium (IV). Anal Biochem 139:487–492

    Article  CAS  PubMed  Google Scholar 

  • Prochazkova D, Sairam RK, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Sci 161:765–771

    Article  CAS  Google Scholar 

  • Rui H, Cao S, Shang H, Jin P, Wang K, Zheng Y (2010) Effects of heat treatment on internal browning and membrane fatty acid in loquat fruit in response to chilling stress. J Sci Food Agr 90:1557–1561

    Article  CAS  Google Scholar 

  • Shomer I, Erner Y (1989) The nature of oleocellosis in citrus fruits. Bot Gaz 150:281–288

    Article  Google Scholar 

  • Sirikesorn L, Ketsa S, van Doorn WG (2013) Low temperature-induced water-soaking of Dendrobium inflorescences: relation with phospholipase D activity, thiobarbaturic-acid-staining membrane degradation products, and membrane fatty acid composition. Postharvest Biol Technol 80:47–55

    Article  CAS  Google Scholar 

  • Smith IK, Vierheller TL, Thorne CA (1988) Assay of glutathione reductase in crude tissue homogenates using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 175:408–413

    Article  CAS  PubMed  Google Scholar 

  • Song LL, Liu H, You YL, Sun J, Yi C, Li YB, Jiang YM, Wu JS (2014) Quality deterioration of cut carnation flowers involves in antioxidant systems and energy status. Sci Hortic-Amsterdam 170:45–52

    Article  CAS  Google Scholar 

  • Sun J, You X, Li L, Peng H, Su W, Li C, He Q, Liao F (2011) Effects of a phospholipase D inhibitor on postharvest enzymatic browning and oxidative stress of litchi fruit. Postharvest Biol Technol 62:288–294

    Article  CAS  Google Scholar 

  • Sun J, Li C, Prasad KN, You X, Li L, Liao F, Peng H, He X, Li Z, Zhang Y (2012) Membrane deterioration, enzymatic browning and oxidative stress in fresh fruits of three litchi cultivars during six-day storage. Sci Hortic-Amsterdam 148:97–103

    Article  CAS  Google Scholar 

  • Tian M, Gu Q, Zhu M (2003) The involvement of hydrogen peroxide and antioxidant enzymes in the process of shoot organogenesis of strawberry callus. Plant Sci 165:701–707

    Article  CAS  Google Scholar 

  • Vitor RF, Lidon FC, Barreiro MG, Maia MI, Medeira MC, Guerreiro A (2001) Peel pitting of Encore mandarin fruits: etiology, control and implications in fruit quality. Fruits 56:27–35

    Article  Google Scholar 

  • Wang Q, Ding T, Zuo J, Gao L, Fan L (2016) Amelioration of postharvest chilling injury in sweet pepper by glycine betaine. Postharvest Biol Technol 112:114–120

    Article  CAS  Google Scholar 

  • Wild BL (1998) New method for quantitatively assessing susceptibility of citrus fruit to oleocellosis development and some factors that affect its expression. Anim Prod Sci 38:279–285

    Article  Google Scholar 

  • Wongsheree T, Ketsa S, van Doorn WG (2009) The relationship between chilling injury and membrane damage in lemon basil (Ocimum × citriodourum) leaves. Postharvest Biol Technol 51:91–96

    Article  CAS  Google Scholar 

  • Zheng Y, He S, Yi S, Zhou Z, Mao S, Zhao X, Deng L (2010a) Predicting oleocellosis sensitivity in citrus using VNIR reflectance spectroscopy. Sci Hortic-Amsterdam 125:401–405

    Article  Google Scholar 

  • Zheng Y, He S, Yi S, Zhou Z, Mao S, Zhao X, Deng L (2010b) Characteristics and oleocellosis sensitivity of citrus fruits. Sci Hortic-Amsterdam 123:312–317

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant No. 31471631) and the Projects in the National Science and Technology Pillar Program during the Twelfth Five-year Plan Period (2015BAD16B07).

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Correspondence to Kaifang Zeng.

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Communicated by PK Nagar.

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Zhou, Y., Xu, J., Xie, J. et al. Involvement of membrane degradation in response to oleocellosis induced by exogenous orange oil in citrus fruit. Acta Physiol Plant 39, 163 (2017). https://doi.org/10.1007/s11738-017-2464-z

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  • DOI: https://doi.org/10.1007/s11738-017-2464-z

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